Not all sharks are “swimming noses”: variation in olfactory bulb size in cartilaginous fishes

Abstract

Olfaction is a universal modality by which all animals sample chemical stimuli from their environment. In cartilaginous fishes, olfaction is critical for various survival tasks including localizing prey, avoiding predators, and chemosensory communication with conspecifics. Little is known, however, about interspecific variation in olfactory capability in these fishes, or whether the relative importance of olfaction in relation to other sensory systems varies with regard to ecological factors, such as habitat and lifestyle. In this study, we have addressed these questions by directly examining interspecific variation in the size of the olfactory bulbs (OB), the region of the brain that receives the primary sensory projections from the olfactory nerve, in 58 species of cartilaginous fishes. Relative OB size was compared among species occupying different ecological niches. Our results show that the OBs maintain a substantial level of allometric independence from the rest of the brain across cartilaginous fishes and that OB size is highly variable among species. These findings are supported by phylogenetic generalized least-squares models, which show that this variability is correlated with ecological niche, particularly habitat. The relatively largest OBs were found in pelagic-coastal/oceanic sharks, especially migratory species such as Carcharodon carcharias and Galeocerdo cuvier. Deep-sea species also possess large OBs, suggesting a greater reliance on olfaction in habitats where vision may be compromised. In contrast, the smallest OBs were found in the majority of reef-associated species, including sharks from the families Carcharhinidae and Hemiscyllidae and dasyatid batoids. These results suggest that there is great variability in the degree to which these fishes rely on olfactory cues. The OBs have been widely used as a neuroanatomical proxy for olfactory capability in vertebrates, and we speculate that differences in olfactory capabilities may be the result of functional rather than phylogenetic adaptations.

Notes

Acknowledgments

The authors would like to thank all those who helped with the collection and provision of specimens as well as the number of institutions that facilitated collections, especially members of the Leigh Marine Laboratory at the University of Auckland, C. Duffy, N. Bagley and the crew of the Tangaraoa for deep-sea specimens (NIWA), and members of the Neuroecology Group at the University of Western Australia, especially R. Kempster and C. Kerr. The authors are very grateful for the comments from two anonymous reviewers and J. Fitzpatrick (University of Manchester) for statistical advice. K.E.Y. acknowledges a Sir Keith Murdoch Fellowship from the American-Australian Association and K.E.Y. and S.P.C. acknowledge an Australian Research Council Discovery Grant (DP120102327) for funding. T.J.L. is grateful for the support of N. Troje (Queen’s University) during the preparation of this manuscript.

Supplementary material

Supplementary Figure 1 A nexus file of the phylogenetic tree, showing the evolutionary relationships among the 58 species of sharks, batoids, and holocephalans 5 used in this study. This tree is based on parsimony reconstruction from a range of data sources (e.g. Aschliman et al., 2012; Naylor et al., 2012; Didier, 2012) for the purposes of this study and is not based on molecular data. Since the branch lengths for many taxa were unknown, branches were set to equal 1.0 (Pagel 1992). Unresolved nodes were treated as soft polytomies, with branch lengths between internal nodes set to zero (Purvis and 10 Garland 1993). (TXT 15 kb) (NEX 14 kb)